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Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ.

Schumacher MA, Zeng W
Proc Natl Acad Sci U S A 113 4988-93 (2016)
Related entries: 5haw, 5hsz, 5k58

Cited: 28 times
EuropePMC logo PMID: 27091999

Abstract

Cell division in most prokaryotes is mediated by FtsZ, which polymerizes to create the cytokinetic Z ring. Multiple FtsZ-binding proteins regulate FtsZ polymerization to ensure the proper spatiotemporal formation of the Z ring at the division site. The DNA-binding protein SlmA binds to FtsZ and prevents Z-ring formation through the nucleoid in a process called "nucleoid occlusion" (NO). As do most FtsZ-accessory proteins, SlmA interacts with the conserved C-terminal domain (CTD) that is connected to the FtsZ core by a long, flexible linker. However, SlmA is distinct from other regulatory factors in that it must be DNA-bound to interact with the FtsZ CTD. Few structures of FtsZ regulator-CTD complexes are available, but all reveal the CTD bound as a helix. To deduce the molecular basis for the unique SlmA-DNA-FtsZ CTD regulatory interaction and provide insight into FtsZ-regulator protein complex formation, we determined structures of Escherichia coli, Vibrio cholera, and Klebsiella pneumonia SlmA-DNA-FtsZ CTD ternary complexes. Strikingly, the FtsZ CTD does not interact with SlmA as a helix but binds as an extended conformation in a narrow, surface-exposed pocket formed only in the DNA-bound state of SlmA and located at the junction between the DNA-binding and C-terminal dimer domains. Binding studies are consistent with the structure and underscore key interactions in complex formation. Combined, these data reveal the molecular basis for the SlmA-DNA-FtsZ interaction with implications for SlmA's NO function and underscore the ability of the FtsZ CTD to adopt a wide range of conformations, explaining its ability to bind diverse regulatory proteins.

Articles - 5hbu mentioned but not cited (2)

  1. Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ. Schumacher MA, Zeng W. Proc Natl Acad Sci U S A 113 4988-4993 (2016)
  2. A DNA-Binding Protein Tunes Septum Placement during Bacillus subtilis Sporulation. Brown EE, Miller AK, Krieger IV, Otto RM, Sacchettini JC, Herman JK. J Bacteriol 201 e00287-19 (2019)


Reviews citing this publication (8)

  1. At the Heart of Bacterial Cytokinesis: The Z Ring. Du S, Lutkenhaus J. Trends Microbiol 27 781-791 (2019)
  2. Functional Mechanism of the Efflux Pumps Transcription Regulators From Pseudomonas aeruginosa Based on 3D Structures. Housseini B Issa K, Phan G, Broutin I. Front Mol Biosci 5 57 (2018)
  3. Unite to divide: Oligomerization of tubulin and actin homologs regulates initiation of bacterial cell division. Krupka M, Margolin W. F1000Res 7 235 (2018)
  4. Regulation of Cell Division in Bacteria by Monitoring Genome Integrity and DNA Replication Status. Burby PE, Simmons LA. J Bacteriol 202 e00408-19 (2020)
  5. Regulation of cytokinesis: FtsZ and its accessory proteins. Wang M, Fang C, Ma B, Luo X, Hou Z. Curr Genet 66 43-49 (2020)
  6. FtsZ Interactions and Biomolecular Condensates as Potential Targets for New Antibiotics. Zorrilla S, Monterroso B, Robles-Ramos MÁ, Margolin W, Rivas G. Antibiotics (Basel) 10 254 (2021)
  7. Insights into the assembly and regulation of the bacterial divisome. Cameron TA, Margolin W. Nat Rev Microbiol (2023)
  8. Models versus pathogens: how conserved is the FtsZ in bacteria? Battaje RR, Piyush R, Pratap V, Panda D. Biosci Rep 43 BSR20221664 (2023)

Articles citing this publication (18)

  1. Bacterial FtsZ protein forms phase-separated condensates with its nucleoid-associated inhibitor SlmA. Monterroso B, Zorrilla S, Sobrinos-Sanguino M, Robles-Ramos MA, López-Álvarez M, Margolin W, Keating CD, Rivas G. EMBO Rep 20 e45946 (2019)
  2. Caulobacter PopZ forms an intrinsically disordered hub in organizing bacterial cell poles. Holmes JA, Follett SE, Wang H, Meadows CP, Varga K, Bowman GR. Proc Natl Acad Sci U S A 113 12490-12495 (2016)
  3. CbtA toxin of Escherichia coli inhibits cell division and cell elongation via direct and independent interactions with FtsZ and MreB. Heller DM, Tavag M, Hochschild A. PLoS Genet 13 e1007007 (2017)
  4. Structure of the Z Ring-associated Protein, ZapD, Bound to the C-terminal Domain of the Tubulin-like Protein, FtsZ, Suggests Mechanism of Z Ring Stabilization through FtsZ Cross-linking. Schumacher MA, Huang KH, Zeng W, Janakiraman A. J Biol Chem 292 3740-3750 (2017)
  5. Essential dynamic interdependence of FtsZ and SepF for Z-ring and septum formation in Corynebacterium glutamicum. Sogues A, Martinez M, Gaday Q, Ben Assaya M, Graña M, Voegele A, VanNieuwenhze M, England P, Haouz A, Chenal A, Trépout S, Duran R, Wehenkel AM, Alzari PM. Nat Commun 11 1641 (2020)
  6. TetR-family transcription factors in Gram-negative bacteria: conservation, variation and implications for efflux-mediated antimicrobial resistance. Colclough AL, Scadden J, Blair JMA. BMC Genomics 20 731 (2019)
  7. Structural basis for isoform-specific kinesin-1 recognition of Y-acidic cargo adaptors. Pernigo S, Chegkazi MS, Yip YY, Treacy C, Glorani G, Hansen K, Politis A, Bui S, Dodding MP, Steiner RA. Elife 7 e38362 (2018)
  8. MinC and FtsZ mutant analysis provides insight into MinC/MinD-mediated Z ring disassembly. Park KT, Dajkovic A, Wissel M, Du S, Lutkenhaus J. J Biol Chem 293 5834-5846 (2018)
  9. Molecular Characterization of the Burkholderia cenocepaciadcw Operon and FtsZ Interactors as New Targets for Novel Antimicrobial Design. Trespidi G, Scoffone VC, Barbieri G, Riccardi G, De Rossi E, Buroni S. Antibiotics (Basel) 9 E841 (2020)
  10. Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in Caulobacter crescentus. Ozaki S, Jenal U, Katayama T. mBio 11 e00487-20 (2020)
  11. The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes. Robles-Ramos MÁ, Margolin W, Sobrinos-Sanguino M, Alfonso C, Rivas G, Monterroso B, Zorrilla S. mBio 11 e02094-20 (2020)
  12. A newly identified prophage-encoded gene, ymfM, causes SOS-inducible filamentation in Escherichia coli. Ansari S, Walsh JC, Bottomley AL, Duggin IG, Burke C, Harry EJ. J Bacteriol 203 JB.00646-20 (2021)
  13. An enhancer sequence in the intrinsically disordered region of FtsZ promotes polymer-guided substrate processing by ClpXP protease. Viola MG, Perdikari TM, Trebino CE, Rahmani N, Mathews KL, Pena CM, Chua XY, Xuan B, LaBreck CJ, Fawzi NL, Camberg JL. Protein Sci 31 e4306 (2022)
  14. Intrinsically Disordered Bacterial Polar Organizing Protein Z, PopZ, Interacts with Protein Binding Partners Through an N-terminal Molecular Recognition Feature. Nordyke CT, Ahmed YM, Puterbaugh RZ, Bowman GR, Varga K. J Mol Biol 432 6092-6107 (2020)
  15. Three Microbial Musketeers of the Seas: Shewanella baltica, Aliivibrio fischeri and Vibrio harveyi, and Their Adaptation to Different Salinity Probed by a Proteomic Approach. Kloska A, Cech GM, Nowicki D, Maciąg-Dorszyńska M, Bogucka AE, Markert S, Becher D, Potrykus K, Czaplewska P, Szalewska-Pałasz A. Int J Mol Sci 23 619 (2022)
  16. Connecting sequence features within the disordered C-terminal linker of Bacillus subtilis FtsZ to functions and bacterial cell division. Shinn MK, Cohan MC, Bullock JL, Ruff KM, Levin PA, Pappu RV. Proc Natl Acad Sci U S A 119 e2211178119 (2022)
  17. Structures of the DarR transcription regulator reveal unique modes of second messenger and DNA binding. Schumacher MA, Lent N, Chen VB, Salinas R. Nat Commun 14 7239 (2023)
  18. The Longitudinal Dividing Bacterium Candidatus Thiosymbion Oneisti Has a Natural Temperature-Sensitive FtsZ Protein with Low GTPase Activity. Wang J, Bulgheresi S, den Blaauwen T. Int J Mol Sci 23 3016 (2022)


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